Antimicrobial resistance patterns in Streptococcus dysgalactiae in a One Health perspective

Marte Glambek; Steinar Skrede; Audun Sivertsen; Bård Reiakvam Kittang; Alba Kaci; Christine Monceyron Jonassen; Hannah Joan Jørgensen; Norwegian Study Group on Streptococcus dysgalactiae; Oddvar Oppegaard

doi:10.3389/fmicb.2024.1423762

Antimicrobial resistance patterns in Streptococcus dysgalactiae in a One Health perspective

Front Microbiol. 2024 Jun 6:15:1423762. doi: 10.3389/fmicb.2024.1423762. eCollection 2024.

Authors

Affiliations

¹ Department of Medicine, Haukeland University Hospital, Bergen, Norway.
² Department of Clinical Medicine 2, Department of Clinical Science, University of Bergen, Bergen, Norway.
³ Department of Microbiology, Haukeland University Hospital, Bergen, Norway.
⁴ Department of Internal Medicine, Haraldsplass Deaconess Hospital (HDS), Bergen, Norway.
⁵ Center for Laboratory Medicine, Østfold Hospital, Grålum, Norway.
⁶ Department of Virology, Division of Infection Control and Environmental Health, Norwegian Institute of Public Health, Oslo, Norway.
⁷ Norwegian Veterinary Institute, Ås, Norway.

Abstract

Background: Streptococcus dysgalactiae (SD) is an important pathogen in humans as well as in a broad range of animal species. Escalating rates of antibiotic resistance in SD has been reported in both human and veterinary clinical practice, but the dissemination of resistance determinants has so far never been examined in a One Health Perspective. We wanted to explore the occurrence of zoonotic transmission of SD and the potential for exchange of resistance traits between SD from different host populations.

Methods: We compared whole genome sequences and phenotypical antimicrobial susceptibility of 407 SD isolates, comprising all isolates obtained from human bloodstream infections in 2018 (n = 274) and available isolates associated with animal infections from the years 2018 and 2019 (n = 133) in Norway.

Results: Antimicrobial resistance genes were detected in 70 (26%), 9 (25%) and 2 (2%) of the isolates derived from humans, companion animals and livestock, respectively. Notably, distinct host associated genotypic resistomes were observed. The erm(A) gene was the dominant cause of erythromycin resistance in human associated isolates, whereas only erm(B) and lsa(C) were identified in SD isolates from animals. Moreover, the tetracycline resistance gene tet(O) was located on different mobile genetic elements in SD from humans and animals. Evidence of niche specialization was also evident in the phylogenetic analysis, as the isolates could be almost perfectly delineated in accordance with host species. Nevertheless, near identical mobile genetic elements were observed in four isolates from different host species including one human, implying potential transmission of antibiotic resistance between different environments.

Conclusion: We found a phylogenetic delineation of SD strains in line with host adapted populations and niche specialization. Direct transmission of strains or genetic elements carrying resistance genes between SD from different ecological niches appears to be rare in our geographical region.

Keywords: Norway; One Health; Streptococcus dysgalactiae; animal; antibiotic resistance; horizontal genetic transfer; human; whole genomic sequencing.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the Norwegian surveillance program for antimicrobial resistance (NORM) (Grant number: 19/08, to OO and 19/16 to CJ) and Center for Laboratory Medicine at Østfold Hospital Trust. The genomic Core Facility (GCF) at the University of Bergen, which is part of the NorSeq consortium, provided services on the whole genome sequencing in this study; GCF is supported by major grants from the Research Council of Norway (grant no. 245979/F50) and Trond Mohn Foundation (grant no. BFS2017TMT04/BFS2017TMT08). This study was received also financial contributions from the Western Norway Regional Health Authority (grant no. 912231). SS received grants from the Norwegian Research Council under the frames of NordForsk (Project: 90456, PerAID) and ERA PerMed (Project: 2018-151, PerMIT).